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Stepwise Functional Evolution in a Fungal Sugar Transporter Family Carla Gonçalvesa, Marco A

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Stepwise Functional Evolution in a Fungal Sugar Transporter Family Carla Gonçalvesa, Marco A MBE Advance Access published October 15, 2015 Article Discoveries Section Stepwise functional evolution in a fungal sugar transporter family Carla Gonçalvesa, Marco A. Coelhoa Madalena Salema-Ooma,b and Paula Gonçalvesa,* aUCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Downloaded from Tecnologia, Universidade NOVA de Lisboa, 2829-516, Caparica, Portugal bInstituto Superior Ciências da Saúde Egas Moniz, Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), 2829-511, Caparica, Portugal http://mbe.oxfordjournals.org/ *Corresponding Author: Paula Gonçalves UCIBIO-REQUIMTE Departamento de Ciências da Vida at Egas Moniz - Cooperativa de Ensino Superior, CRL on January 17, 2017 Faculdade de Ciências e Tecnologia Universidade Nova de Lisboa 2829-516, Caparica, Portugal Tel: (+351) 21 294 85 30 Email: [email protected] © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: [email protected] 1 Abstract Sugar transport is of the utmost importance for most cells and is important to a wide range of applied fields. However, despite the straightforward in silico assignment of many novel transporters, including sugar porters, to existing families, their exact biological role and evolutionary trajectory often remain unclear, mainly because biochemical characterization of membrane proteins is inherently challenging, but also owing to their uncommonly turbulent evolutionary histories. In addition, many important shifts in membrane carrier function are Downloaded from apparently ancient, which further limits our ability to reconstruct evolutionary trajectories in a reliable manner. Here we circumvented some of these obstacles by examining the relatively recent emergence of http://mbe.oxfordjournals.org/ a unique family of fungal sugar facilitators, related to drug antiporters. The former transporters, named Ffz, were previously shown to be required for fructophilic metabolism in yeasts. We first exploited the wealth of fungal genomic data available to define a comprehensive but well- delimited family of Ffz-like transporters, showing that they are only present in Dikarya. Subsequently, a combination of phylogenetic analyses and in vivo functional characterization was used to retrace important changes in function, while highlighting the evolutionary events that are at Egas Moniz - Cooperativa de Ensino Superior, CRL on January 17, 2017 most likely to have determined extant distribution of the gene, such as horizontal gene transfers (HGTs). One such HGT event is proposed to have set the stage for the onset of fructophilic metabolism in yeasts, a trait that according to our results may be the metabolic hallmark of approximately one hundred yeast species that thrive in sugar rich environments. 2 Introduction Sugar transport is a biological process of paramount importance, since for a wide variety of organisms in all kingdoms of life, sugars (mono and di-saccharides) are favorite carbon and energy sources. Partitioning and distribution of sugars is accordingly found to be disturbed in various important animal and plant diseases. For example, one important biochemical hallmark of cancer cells is their increased rates of glucose uptake (Ganapathy-Kanniappan and Geschwind Downloaded from 2013) and some bacterial plant pathogens are able to increase sugar levels in their vicinity by inducing the expression of particular sugar transporter genes in the host plant (Streubel et al. 2013). Moreover, industrial substrates for microbial growth are often sugar-rich and research on http://mbe.oxfordjournals.org/ microbial biotechnology based processes, such as beer and bioethanol production, revealed over the past few decades several examples of the high impact of the sugar transport step on overall fermentation performances (Reznicek et al. 2015; Vidgren et al. 2010; Young et al. 2012). This was also patent when domesticated microbes were genetically dissected and compared to their “wild counterparts” (Libkind et al. 2011; Perez-Ortin et al. 2002). Hence, an improved understanding of sugar transport is pertinent to a wide variety of areas of applied interest, from at Egas Moniz - Cooperativa de Ensino Superior, CRL on January 17, 2017 human health to agricultural crop yield and biotechnology. In spite of this, the elucidation of functional and structural aspects of integral membrane proteins, remains inherently challenging, resulting in a considerable deficit in available biochemical data for in silico predicted transporter proteins, when compared to their soluble metabolic enzyme counterparts (Reddy et al. 2012). While approximately 800 families of cellular solute transporters have been identified, based on functional and phylogenetic evidence (Saier et al. 2014), most eukaryotic sugar carriers belong to the largest superfamily of transporters, the so-called Major Facilitator Superfamily (MFS) (Pao et al. 1998). This superfamily is ubiquitously distributed in the biosphere, and is characterized on the one hand by considerable structural conservation and, on the other hand, by an astounding diversity of substrates and of modes of operation (uniport, symport and antiport) (Reddy, et al. 2012). The few sugar transporters that do not belong to MFS are a well-studied human glucose transporter (SGLT) placed in the solute:sodium symporter family (Wright et al. 2011) and a novel type of carrier generically dubbed SWEET (or SemiSWEET) that was recently discovered in plants, animals and bacteria and fits into the Transporter-Opsin-G-protein coupled receptor (TOG) superfamily (Feng and Frommer 2015). In fungi, all sugar transporters characterized so far are included in the Sugar Porter (SP) family within MFS, with the notable exception of those belonging to the Ffz-like family which are the main subject of this work (Leandro et al. 2011) and were rather included in a different MFS family formed by Drug:H+ antiporters (DHA1 family). 3 Ffz transporters have so far been found only in a limited number of fungal species (Cabral et al. 2015; Leandro, et al. 2011; Lee et al. 2014; Pina et al. 2004). In vivo biochemical characterization showed that they are usually high capacity and low affinity uniporters, specific for fructose (Leandro, et al. 2011; Lee, et al. 2014; Pina, et al. 2004), while genetic analyses showed that Ffz1 seems to be a pre-requisite for fructophily in at least one yeast species (Leandro et al. 2014). Fructophily, defined as the preference for fructose over glucose as carbon and energy source, is a metabolic trait well characterized so far in a few yeast species found in high sugar environments (Pina, et al. 2004; Tofalo et al. 2009) and in some bacteria (Endo et al. 2009; Endo Downloaded from and Salminen 2013). The singularity of the evolutionary origin of the Ffz family of transporters and its consistent association with fructophily in yeast taxa belonging to widely different lineages but inhabiting similar habitats (Sousa-Dias et al. 1996; Yu et al. 2006), suggest an evolutionary http://mbe.oxfordjournals.org/ path punctuated by profound but relatively recent functional change and opens the possibility to establish a link between functional evolution and certain ecological traits. In fact, the organization of transporter families within the MFS Superfamily shows a general agreement between phylogenetic relatedness and the type of substrate accepted by the transporter. For example, the Most Recent Common Ancestor (MRCA) of the Sugar Porter family probably goes far back in evolutionary history, as this family comprises members spanning the diversity of life, from human at Egas Moniz - Cooperativa de Ensino Superior, CRL on January 17, 2017 to bacteria, all accepting only sugars or related compounds as substrates. Hence, the emergence of a sugar transporter “sub-family” within a Drug:H+ antiporter family is likely to be comparatively a very recent event, possibly related to selective pressures associated to the adaptation of specific fungal lineages to new environments or lifestyles. In addition, within the Ffz family itself, some functional differences have been noted prior to this study, since the Ffz2 type of transporter accepts both glucose and fructose as substrates (Leandro, et al. 2011) contrary to the first identified member of the family, Ffz1, reported to accept only fructose (Pina, et al. 2004). All these considerations led us to regard the Ffz family as an excellent model in which to examine adaptive evolution of transporters and possibly to establish a relation between sugar transport and organismal ecology. As a consequence, we set out to explore the wealth of genomic data available for fungi to illuminate the evolutionary origin and history of the Ffz sugar transporter family. Elucidation of the molecular evolution of sugar transporters is often complicated by redundancy and particularly rapid evolution (Brown et al. 2010; Lin and Li 2011). An emblematic example of this is the small genome of the model yeast Saccharomyces cerevisiae that encodes at least 17 hexose uniporters, named HXT. Biochemical characterization revealed similar substrate specificities for many of the Hxt transporters but clear differences in the affinity for glucose (Diderich et al. 2001; Reifenberger et al. 1997). However, provided that expression levels are appropriate, most HXT genes seem to be able to support growth of S. cerevisiae on glucose, fructose and mannose (Diderich, et al. 2001; Reifenberger, et
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